Intracellular concentrations of 65 species of transcription factors with known regulatory functions in Escherichia coli

Journal of Bacteriology

Volumn 196, Issue 15, 2014, Pages 2718-2727

  Ishihama, Akira ^a,b,c   Kori, Ayako ^a,b   Koshio, Etsuko ^c   Yamada, Kayoko ^a,b   Maeda, Hiroto ^c,d   Shimada, Tomohiro ^a,b,e   Makinoshima, Hideki ^b,f   Iwata, Akira ^b   Fujitac, Nobuyuki ^c,g  

^a HOSEI UNIVERSITY   (Japan)

^b NIPPON INSTITUTE FOR BIOLOGICAL SCIENCE   (Japan)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d KAGOSHIMA UNIVERSITY   (Japan)

^e TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^f NATIONAL CANCER CENTER HOSPITAL EAST   (Japan)

^g NATIONAL INSTITUTE OF TECHNOLOGY AND EVALUATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

SIGMA FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL LEVEL; CONTROLLED STUDY; ESCHERICHIA COLI K 12; GENE EXPRESSION SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; REGULATORY MECHANISM; TEMPERATURE DEPENDENCE; TRANSCRIPTION REGULATION; WILD TYPE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIBODIES, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; INTRACELLULAR SPACE; PROMOTER REGIONS, GENETIC; RABBITS; SEQUENCE DELETION; SIGMA FACTOR; STRESS, PHYSIOLOGICAL; TEMPERATURE; TRANSCRIPTION FACTORS;

EID: 84903906206     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01579-14     Document Type: Article

References (74)

1. Ishihama A. 2010. Prokaryotic genome regulation: multi-factor promoters, multi-target regulators and hierarchic networks. FEMS Microbial. Rev. 34: 628-645. http://dx.doi.org/10.1111/j.1574-6976.2010.00227.x.
2. Ishihama A. 2012. Prokaryotic genome regulation: a revolutionary paradigm. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 88: 485-508. http://dx.doi.org/10.2183/pjab.88.485.
3. Hayashi K, Morooka N, Yamamoto Y, Fujita K, Isono K, Chi S, Ohtsubo E, Baba T, Wanner BL, Mori H, Horiuchi T. 2006. Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol. Syst. Biol. 2: 2006.0007. http://dx.doi.org/10.1038/msb4100049.
4. Riley M, Abe T, Arnaud MB, Berlyn MKB, Blattner FR, Chaudhuri RR, Glasner JD, Horiuchi T, Keseler IM, Kosuge T, Mori H, Perna NT, Plunkett G, III, Rudd KE, Serres MH, Thomas GH, Thomson NR, Wishart D, Wanner BL. 2006. Escherichia coli K-12: a cooperatively developed annotation snapshot-2005. Nucleic Acids Res. 34: 1-9. http://dx .doi.org/10.1093/nar/gkj405.
5. Dornenburg JE, DeVita AM, Palumbo MJ, Wade JT. 2010. Widespread antisense transcription in Escherichia coli. mBio 1(1): e00024-10. http://dx .doi.org/10.1128/mBio.00024-10.
6. Oh M-K, Rohlin L, Kao KC, Liao JC. 2002. Global expression profiling of acetate-grown Escherichia coli. J. Biol. Chem. 277: 13175-13183. http://dx.doi.org/10.1074/jbc.M110809200.
7. Richmond CS, Glasner JD, Mau R, Jin H, Blattner F. 1999. Genomewide expression profiling in Escherichia coli K-12. Nucleic Acids Res. 27: 3821-3835. http://dx.doi.org/10.1093/nar/27.19.3821.
8. Phadtare S, Inouye M. 2004. Genome-wide transcriptional analysis of the cold-shock response in wild-type and cold-sensitive, quadruple-cspdeletion strains of Escherichia coli. J. Bacteriol. 186: 7007-7914. http://dx .doi.org/10.1128/JB.186.20.7007-7014.2004.
9. Zheng M, Wang X, Templeton LJD, Smulski R, LaRossa RA, Storz G. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183: 4562-4570. http://dx.doi.org/10.1128/JB.183.15.4562-4570.2001.
10. Lee LJ, Barrett JA, Poole RK. 2005. Genome-wide transcriptional response to chemostat-cultured Escherichia coli to zinc. J. Bacteriol. 187: 1124-1134. http://dx.doi.org/10.1128/JB.187.3.1124-1134.2005.
11. Overton TW, Griffiths L, Patel MD, Hobman JL, Penn CW, Cole JA, Constantinidou C. 2006. Microarray analysis of gene regulation by oxygen, nitrate, nitrite, FNR, NarL and NarP during anaerobic growth of Escherichia coli: new insights into microbial physiology. Biochem. Soc. Transact. 34: 104-107. http://dx.doi.org/10.1042/BST0340104.
12. Ren D, Bedzyk LA, Thomas SM, Ye RW, Wood TK. 2004. Gene expression in Escherichia coli biofilms. Appl. Microbiol. Biotechnol. 64: 515-524. http://dx.doi.org/10.1007/s00253-003-1517-y.
13. Cho BK, Zengler K, Qiu Y, Park YS, Knight EM, Barrett CL, Gao Y, Palsson BO. 2009. The transcriptome unit architecture of the Escherichia coli genome. Nat. Biotechnol. 27: 1043-1049. http://dx.doi.org/10.1038/nbt.1582.
14. Raghavan R, Sage A, Ochman H. 2011. Genome-wide identification of transcription start sites yields a novel thermosensing RNA and new cyclic AMP receptor protein-regulated genes in Escherichia coli. J. Bacteriol. 193: 2871-2874. http://dx.doi.org/10.1128/JB.00398-11.
15. Ginnoukos G, Ciulla DM, Huang K, Haas BJ, Izard J, Levin JZ, Livny J, Earl AM, Gevers D, Yard DV, Husbaum C, Birren BW, Gnirke A. 2012. Efficient and robust RNA-seq process for cultured bacteria and complex community transcriptomes. Genome Biol. 13: r23.70. http://dx .doi.org/10.1186/gb-2012-13-3-r23.
16. Ishihama A. 2000. Functional modulation of Escherichia coli RNA poly-merase. Annu. Rev. Microbiol. 54: 499-518. http://dx.doi.org/10.1146/annurev.micro.54.1.499.
17. Peruz-Rueda E, Collado-Vides J. 2000. The repertoire of DNA-binding transcription regulators in Escherichia coli K-12. Nucleic Acids Res. 28: 1838-1847. http://dx.doi.org/10.1093/nar/28.8.1838.
18. Herring CD, Raffaelle M, Allen TE, Kanin EI, Landick R, Ansari AZ, Palsson BO. 2005. Immobilization of Escherichia coli RNA polymerase and location of binding sites by use of chromatin immunoprecipitation and microarrays. J. Bacteriol. 187: 6166-6174. http://dx.doi.org/10.1128/JB.187.17.6166-6174.2005.
19. Mooney RA, Davis SE, Peters JM, Rowland JL, Ansari AZ, Landick R. 2009. Regulator trafficking on bacterial transcription units in vivo. Mol. Cell 33: 97-108. http://dx.doi.org/10.1016/j.molcel.2008.12.021.
20. Shimada T, Fujita N, Maeda M, Ishihama A. 2005. Systematic search for the Cra-binding promoters using genomic SELEX. Genes Cells 10: 907-918. http://dx.doi.org/10.1111/j.1365-2443.2005.00888.x.
21. Shimada T, Yamazaki Y, Tanaka K, Ishihama A. 2014. The whole set of constitutive promoters recognized by RNA polymerase RpoD holoenzyme of Escherichia coli. PLoS One 9(3): e90447. http://dx.doi.org/10.1371/journal.pone.0090447.
22. Shimada K, Ogasawara H, Yamada K, Shimura M, Kori A, Shimada T, Yamanaka Y, Yamamoto K, Ishihama A. 2013. Screening of promoterspecific transcription factors: multiple regulators for the sdiA gene involved in cell division control and quorum sensing. Microbiology 159: 2501-2512. http://dx.doi.org/10.1099/mic.0.067538-0.
23. Salgado H, Peralta-Gil M, Gama-Castro S, Santos-Zavaleta A, Munz-Rascado L, Garcia-Sotelo JS, Wess V, Solano-Lira H, Martinez-Flores I, Medina-Rivera A, Salgado-Osorio S, Alqicira-Hermandez S, Alquicira-Hernandez K, Lopez-Fuentes A, Porron-Sotelo L, Huerta AM, Bonavides-Martinez C, Balderas-Martinez YI, Pannier L, Olvera M, Labastida A, Jimenez-Jacinto V, Vega-Alvarado L, del Moral-Chavex V, Hernandez-Alvarez A, Morett E, Collado-Vides J. 2012. RegullonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more. Nucleic Acids Res. 41: D203-D213. http://dx.doi.org/10.1093/nar/gks1201.
24. Keseler IM, Kackie A, Peralta-Gil M, Santos-Zavalete A, Gama-Castro S, Bonavides-Martinez C, Fulcher C, Huerta AM, Kothari A, Krummenacker M, Latendresse M, Muniz-Rascado L, Ong Q, Paley S, Schroder I, Shearer AG, Subhraveti P, Travers M, Weerasinghe D, Weiss V, Collado-Vides J, Gunslus RP, Paulsen I, Karp PD. 2012. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res. 41: D605-D612. http://dx.doi.org/10.1093/nar/gks1027.
25. Gunsalus RP, Miguel AG, Gunsalus GL. 1986. Intracellular Trp repressor levels in Escherichia coli. J. Bacteriol. 167: 272-278.
26. Borst DW, Blumenthal RM, Mattews RG. 1996. Use of an in vitro titration method to study a global regulator: effects of varying Lrp levels on expression of gltBDF in Escherichia coli. J. Bacteriol. 178: 6904-6912.
27. Jishage M, Ishihama AA. 1995. Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of σ70 and σ38. J. Bacteriol. 177: 6832-6835.
28. Jishage M, Iwata A, Ueda S, Ishihama A. 1996. Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma subunit under various growth conditions. J. Bacteriol. 178: 5447-5451.
29. Maeda H, Jishage M, Nomura T, Fujita N, Ishihama A. 2000. Promoter selectivity of the RNA polymerase holoenzyme containing the extracytoplasmic function (ECF) sigma subunit, sigma-E and FecI. J. Bacteriol. 182: 1181-1184. http://dx.doi.org/10.1128/JB.182.4.1181-1184.2000.
30. Jishage M, Ishihama A. 1997. Variation in RNA polymerase sigma subunit composition within different stocks of Escherichia coli W3110. J. Bacteriol. 179: 959-963.
31. Baba T, Ara T, Hasgawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2: 20006.0006. http://dx.doi.org/10.1038/msb4100050.
32. Yamamoto K, Hirao K, Ohshima T, Aiba H, Utsumi R, Ishihama A. 2005. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 280: 1448-1456. http://dx.doi.org/10.1074/jbc.M410104200.
33. Martinez-Antonio A, Collado-Vides J. 2003. Identifying global regulators in transcriptional regulatory networks in bacteria. Curr. Opin. Microbiol. 6: 482-489. http://dx.doi.org/10.1016/j.mib.2003.09.002.
34. Ishihama A. 2009. The nucleoid: an overview. In Boek A, Curtiss R, III, Kaper JB, Karp PD, Neidhardt FC, Nystrom T, Slauch JM, Squires CL, Ussery D (ed). EcoSal-Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC.
35. Finkel ES, Johnson RC. 1992. The Fis protein: it's not just for DNA inversion anymore. Mol. Microbiol. 6: 3257-3265. http://dx.doi.org/10 .1111/j.1365-2958.1992.tb02193.x.
36. Cho BK, Knight EM, Barrett CL, Palsson BO. 2008. Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res. 18: 900-910. http://dx.doi.org/10.1101/gr .070276.107.
37. Browning DF, Grainger DC, Busby SJ. 2010. Effects of nucleoidassociated proteins on bacterial chromosome structure and gene expression. Curr. Opin. Microbiol. 13: 773-780. http://dx.doi.org/10.1016/j.mib .2010.09.013.
38. Teramoto J, Yoshimura SH, Takeysu K, Ishihama A. 2010. A novel nucleoid protein of Escherichia coli induced under anaerobic growth conditions. Nucleic Acids Res. 38: 3605-3618. http://dx.doi.org/10.1093/nar/gkq077.
39. Almiron M, Link AJ, Furlong D, Kolter R. 1992. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6: 2646-2654. http://dx.doi.org/10.1101/gad.6.12b.2646.
40. Leonard AC, Grimwade JE. 2011. Regulation of DnaA assembly and activity: taking directions from the genome. Annu. Rev. Microbiol. 65: 19-35. http://dx.doi.org/10.1146/annurev-micro-090110-102934.
41. Balderas-Martinez YI, Savageau M, Saldago H, Perez-Rueda E, Morett E, Collado-Vides J. 2013. Transcription factors in Escherichia coli prefer the holo conformation. PLoS One 8: e65723. http://dx.doi.org/10.1371/journal.pone.0065723.
42. Hantke K. 2001. Iron and metal regulation in bacteria. Curr. Opin. Microbiol. 4: 172-177. http://dx.doi.org/10.1016/S1369-5274(00)00184-3.
43. Kang Y, Weber KD, Qiu Y, Kiley PJ, Blattner FR. 2005. Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J. Bacteriol. 187: 1135-1160. http://dx.doi.org/10.1128/JB.187.3.1135-1160.2005.
44. Iuchi S, Weiner L. 1996. Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments. J. Biochem. 120: 1055-1063. http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021519.
45. Minagawa S, Ogasawara H, Kato A, Yamamoto K, Eguchi Y, Oshima T, Mori H, Ishihama A, Utsumi R. 2003. Identification and characterization of the Mg2+ stimulon of Escherichia coli. J. Bacteriol. 185: 3696-3702. http://dx.doi.org/10.1128/JB.185.13.3696-3702.2003.
46. Wanner BL. 1993. Gene regulation by phosphate in enteric bacteria. J. Cell. Biochem. 51: 47-54. http://dx.doi.org/10.1002/jcb.240510110.
47. Shimada T, Fujita N, Yamamoto K, Ishihama AA. 2011. Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. PLoS One 6: e20081. http://dx.doi.org/10.1371/journal .pone.0020081.
48. Shimada T, Yamamoto K, Ishihama A. 2011. Novel members of the Cra regulon involved in carbon metabolism in Escherichia coli. J. Bacteriol. 193: 649-659. http://dx.doi.org/10.1128/JB.01214-10.
49. Calvo JM, Matthews RG. 1994. The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol. Rev. 58: 466-490.
50. Shimada T, Bridier A, Briandet R, Ishihama A. 2011. Novel roles of LeuO in transcription regulation in E. coli: antagonistic interplay with the universal silencer H-NS. Mol. Microbiol. 82: 376-397. http://dx.doi.org/10.1111/j.1365-2958.2011.07818.x.
51. Shimada T, Hirao K, Kori A, Yamamoto K, Ishihama A. 2007. RutR is the uracil/thymine-sensing master regulator of a set of genes for synthesis and degradation of pyrimidines. Mol. Microbiol. 66: 744-757. http://dx .doi.org/10.1111/j.1365-2958.2007.05954.x.
52. Rintoul MR, Cusa E, Baldoma L, Badia J, Reitzer L, Aguilar J. 2002. Regulation of the Escherichia coli allantoin regulon: coordinated function of the repressor AllR and the activator AllS. J. Mol. Biol. 324: 599-610. http://dx.doi.org/10.1016/S0022-2836(02)01134-8.
53. Masiewicz P, Brzostek A, Wolanski M, Dziadek J, Zakrzewska-Czerwinska J. 2012. A novel role of the RppR as a transcription factor involved in the regulation of methylcitrate pathway in Mycobacterium tuberculosis. PLoS One 8: e43651.
54. Shimada T, Shimada K, Matsui M, Kitai Y, Igarashi J, Suga H, Ishihama A. 2014. Roles of cell division control factor SdiA: recognition of quorum sensing signals and modulation of transcription regulation targets. Genes Cells 19: 405-418. http://dx.doi.org/10.1111/gtc.12139.
55. Shimada T, Katayama Y, Kawakita S, Ogasawara H, Nakano M, Yamanaka K, Ishihama A. 2012. A novel regulator RcdA of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli. Microbiologyopen 1: 381-394. http://dx.doi.org/10.1002/mbo3.42.
56. Azam TA, Iwata A, Nishimura A, Ueda S, Ishihama A. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181: 6361-6370.
57. Nair S, Finkel SE. 2004. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 186: 4192-4198. http://dx.doi.org/10.1128/JB.186.13.4192-4198.2004.
58. Oshima T, Biville F. 2006. Functional identification of ygiP as a positive regulator of the ttdA-ttdB-ygjE operon. Microbiology 152: 2129-2135. http://dx.doi.org/10.1099/mic.0.28753-0.
59. Garcia-Lara J, Shang LH, Rothfield LI. 1996. An extracellular factor regulates expression of sdiA, a transcriptional activator of cell division genes in Escherichia coli. J. Bacteriol. 178: 2742-2748.
60. Rudolph B, Gebendorfer KM, Buchner J, Winter J. 2010. Evolution of Escherichia coli for growth at high temperatures. J. Biol. Chem. 285: 19029-19034. http://dx.doi.org/10.1074/jbc.M110.103374.
61. Guisbert E, Yura T, Rhodius VA, Gross CA. 2008. Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microb. Mol. Biol. Rev. 72: 545-554. http://dx.doi.org/10.1128/MMBR.00007-08.
62. Zhang A, Rimsky S, Reaban ME, Buc H, Belfort M. 1996. Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J. 15: 1340-1349.
63. Cullum AJ, Bennett AF, Lenski RE. 2001. Evolutionary adaptation to temperature. IX. Preadaptation to novel stressful environments of Escherichia coli adapted to high temperature. Evolution 55: 2194-2202.
64. Travisano M, Lenski RE. 1996. Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics 143: 15-26.
65. Barria C, Malecki M, Arraiano CM. 2013. Bacterial adaptation to cold. Microbiology 159: 2437-2443. http://dx.doi.org/10.1099/mic.0.052209-0.
66. White-Ziegler CA, Um S, Perez NM, Berns AL, Malhowski AJ, Young S. 2008. Low temperature (23° C) increases expression of biofilm-, coldshock-, and RpoS-dependent genes in Escherichia coli K-12. Microbiology 154: 148-166. http://dx.doi.org/10.1099/mic.0.2007/012021-0.
67. Browning DF, Busby SJ. 2004. The regulation of bacterial transcription initiation. Nat. Rev. Microbiol. 2: 57-65. http://dx.doi.org/10 .1038/nrmicro787.
68. Thao S, Chen C-S, Zhu H, Escalante-Semerena JC. 2010. N-Lysine acetylation of a bacterial transcription factor inhibits its DNA-binding activity. PLoS One 5: e15123. http://dx.doi.org/10.1371/journal.pone .0015123.
69. Yu BJ, Kim JA, Moon JH, Ryu SE, Pan J-G. 2008. Diversity of lysineacetylated proteins in Escherichia coli. J. Microbiol. Biotechnol. 18: 1529-1536.
70. Alix JH. 1988. Post-translational methylations of ribosomal proteins. Adv. Exp. Med. Biol. 231: 371-385.
71. Sakumi K, Igarashi K, Sekiguchi M, Ishihama A. 1993. The Ada protein is a class I transcription factor of Escherichia coli. J. Bacteriol. 175: 2455-2457.
72. Kang WK, Icho T, Isono S, Kitakawa M, Isono K. 1989. Characterization of the gene rimK responsible for the addition of glutamic acid residues to the C-terminus of ribosomal protein S6 in Escherichia coli K-12. Mol. Gen. Genet. 217: 281-288. http://dx.doi.org/10.1007/BF02464894.
73. Ding H, Demple B. 2011. Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. U. S. A. 97: 5146-5150. http://dx.doi.org/10.1073/pnas.97.10.5146.
74. Seth D, Hausladen A, Wang Y-J, Stampler JS. 2012. Endogenous protein S-nitrosylation in E. coli: regulation by OxyR. Science 336: 470-473. http://dx.doi.org/10.1126/science.1215643.